Conceptual learning by miniature brains

Concepts act as a cornerstone of human cognition. Humans and non-human primates learn conceptual relationships such as ‘same’, ‘different’, ‘larger than’, ‘better than’, among others. In all cases, the relationships have to be encoded by the brain independently of the physical nature of objects linked by the relation. Consequently, concepts are associated with high levels of cognitive sophistication and are not expected in an insect brain. Yet, various works have shown that the miniature brain of honeybees rapidly learns conceptual relationships involving visual stimuli. Concepts such as ‘same’, ‘different’, ‘above/below of’ or ‘left/right are well mastered by bees. We review here evidence about concept learning in honeybees and discuss both its potential adaptive advantage and its possible neural substrates. The results reviewed here challenge the traditional view attributing supremacy to larger brains when it comes to the elaboration of concepts and have wide implications for understanding how brains can form conceptual relations.     

Information processing in miniature brains

Since a comprehensive understanding of brain function and evolution in vertebrates is often hobbled by the sheer size of the nervous system, as well as ethical concerns, major research efforts have been made to understand the neural circuitry underpinning behaviour and cognition in invertebrates, and its costs and benefits under natural conditions. This special feature of Proceedings of the Royal Society B contains an idiosyncratic range of current research perspectives on neural underpinnings and adaptive benefits (and costs) of such diverse phenomena as spatial memory, colour vision, attention, spontaneous behaviour initiation, memory dynamics, relational rule learning and sleep, in a range of animals from marine invertebrates with exquisitely simple nervous systems to social insects forming societies with many thousands of individuals working together as a 'superorganism'. This introduction provides context and history to tie the various approaches together, and concludes that there is an urgent need to understand the full neuron-to-neuron circuitry underlying various forms of information processing-not just to explore brain function comprehensively, but also to understand how (and how easily) cognitive capacities might evolve in the face of pertinent selection pressures. In the invertebrates, reaching these goals is becoming increasingly realistic.     

Desert ant navigation: how miniature brains solve complex tasks

This essay presents and discusses the state of the art in studies of desert ant (Cataglyphis) navigation. In dealing with behavioural performances, neural mechanisms, and ecological functions these studies ultimately aim at an evolutionary understanding of the insect's navigational toolkit: its skylight (polarization) compass, its path integrator, its view-dependent ways of recognizing places and following landmark routes, and its strategies of flexibly interlinking these modes of navigation to generate amazingly rich behavioural outputs. The general message is that Cataglyphis uses path integration as an egocentric guideline to acquire continually updated spatial information about places and routes. Hence, it relies on procedural knowledge, and largely context-dependent retrieval of such knowledge, rather than on all-embracing geocentred representations of space.This revised version was published online in July 2003 with corrections to the text of the sections "Skylight compass" and "Path integration".     

Disrupted in schizophrenia 1: building brains and memories

Schizophrenia and bipolar affective disorder are common, debilitating, and poorly understood and treated disorders. Both conditions are highly heritable. Recent genetic studies have suggested that the gene disrupted in schizophrenia 1 (DISC1) is an important risk factor. DISC1 seems to have a key role in building the brain and memories by interacting with other proteins, including nuclear distribution E-like protein and phosphodiesterase 4B. Here, we review the current knowledge, highlight some key unanswered questions and propose ways forward towards a better understanding of normal and abnormal brain development and function. In the long term, this might lead to the discovery of drugs that are more efficacious and safer than currently available ones.     

A blueprint for vocal learning: auditory predispositions from brains to genomes

Memorizing and producing complex strings of sound are requirements for spoken human language. We share these behaviours with likely more than 4000 species of songbirds, making birds our primary model for studying the cognitive basis of vocal learning and, more generally, an important model for how memories are encoded in the brain. In songbirds, as in humans, the sounds that a juvenile learns later in life depend on auditory memories formed early in development. Experiments on a wide variety of songbird species suggest that the formation and lability of these auditory memories, in turn, depend on auditory predispositions that stimulate learning when a juvenile hears relevant, species-typical sounds. We review evidence that variation in key features of these auditory predispositions are determined by variation in genes underlying the development of the auditory system. We argue that increased investigation of the neuronal basis of auditory predispositions expressed early in life in combination with modern comparative genomic approaches may provide insights into the evolution of vocal learning.     

Social learning in cooperative dilemmas

Helping is a cornerstone of social organization and commonplace in human societies. A major challenge for the evolutionary sciences is to explain how cooperation is maintained in large populations with high levels of migration, conditions under which cooperators can be exploited by selfish individuals. Cultural group selection models posit that such large-scale cooperation evolves via selection acting on populations among which behavioural variation is maintained by the cultural transmission of cooperative norms. These models assume that individuals acquire cooperative strategies via social learning. This assumption remains empirically untested. Here, I test this by investigating whether individuals employ conformist or payoff-biased learning in public goods games conducted in 14 villages of a forager–horticulturist society, the Pahari Korwa of India. Individuals did not show a clear tendency to conform or to be payoff-biased and are highly variable in their use of social learning. This variation is partly explained by both individual and village characteristics. The tendency to conform decreases and to be payoff-biased increases as the value of the modal contribution increases. These findings suggest that the use of social learning in cooperative dilemmas is contingent on individuals'' circumstances and environments, and question the existence of stably transmitted cultural norms of cooperation.     

Social learning and teaching in chimpanzees

There is increasing evidence that some behavioural differences between groups of chimpanzees can be attributed neither to genetic nor to ecological variation. Such differences are likely to be maintained by social learning. While humans teach their offspring, and acquire cultural traits through imitative learning, there is little evidence of such behaviours in chimpanzees. However, by appealing only to incremental changes in motivation, attention and attention-soliciting behaviour, and without expensive changes in cognition, we can hypothesise the possible emergence of imitation and pedagogy in evolutionary history.     

Social learning: public information in insects

Although it has received less coverage than in vertebrates, the study of insect social learning has a rich history with spectacular examples of how individuals extract knowledge from other animals. Several new studies on crickets and social bees have now shown how insects can adjust their behaviour adaptively by making use of cues generated inadvertently by other individuals.     

Social learning about egg-laying substrates in fruitflies

Social learning, defined as learning from other individuals, has had dramatic effects on some species, including humans, in whom it has generated a rich culture. As a first step in examining the evolution of and mechanisms underlying social learning in insects, we tested for social learning in fruitflies (Drosophila melanogaster). Focal females (observers) that experienced novel food together with mated females (models), who had laid eggs on that food, subsequently exhibited a stronger preference for laying eggs on that food over another novel food compared with focal females that experienced the food alone. We observed no social learning, however, when observers experienced food with potentially more ambiguous social information provided by the presence of either virgin models or aggregation pheromone. This first documentation of social learning about egg-laying substrates in fruitflies builds on recent data indicating intricate use of social information by fruitflies and opens up exciting avenues for research on the evolution and neurogenetics of social learning using biology''s major model system.     

Social learning among Congo Basin hunter-gatherers

This paper explores childhood social learning among Aka and Bofi hunter-gatherers in Central Africa. Existing literature suggests that hunter-gatherer social learning is primarily vertical (parent-to-child) and that teaching is rare. We use behavioural observations, open-ended and semi-structured interviews, and informal and anecdotal observations to examine the modes (e.g. vertical versus horizontal/oblique) and processes (e.g. teaching versus observation and imitation) of cultural transmission. Cultural and demographic contexts of social learning associated with the modes and processes of cultural transmission are described. Hunter-gatherer social learning occurred early, was relatively rapid, primarily vertical under age 5 and oblique and horizontal between the ages of 6 and 12. Pedagogy and other forms of teaching existed as early as 12 months of age, but were relatively infrequent by comparison to other processes of social learning such as observation and imitation.     

Social learning in common ravens, Corvus corax

We conducted an experiment to investigate whether the presence of a conspecific model can promote the acquisition of a motor task in common ravens. For this purpose, dyads, either of control birds or of model-observer pairings, were allowed to operate together in an arena with a set of identical boxes. Each box consisted of two compartments each containing a reward of three pieces of meat. The compartments were closed by gliding lids with red flaps on their front, opening horizontally in opposite directions. Naive control individuals opened the lids exclusively by levering, that is, jumping on top of the box, inserting the beak at the posterior rim of the lid and pushing it open. Models were trained to demonstrate an alternative opening technique, pulling at the front flap, then jumping on top of the box to get at the reward. In contrast to the control birds, observers initially opened boxes both ways, by pulling and levering. Furthermore, observers approached the boxes more quickly and showed less fearful behaviour than the control birds, which we attribute to the enhancing effect of the model. We discuss both stimulus enhancement and motor imitation as possible learning mechanisms. Even though observers initially obtained a considerable amount of reward produced by the models, scrounging evidently did not inhibit learning. Copyright 1999 The Association for the Study of Animal Behaviour.     

Left-right development from embryos to brains

Bilateran animals have external bilateral symmetry along the dorsoventral (DV) and anteroposterior (AP) axes. Internal left-right asymmetries appear to be consistently aligned along the left-right (LR) axis with respect to the other axes. Left-right development is most apparent in the directional looping of the cardiac tube, the coiling and placement of the intestines, the positioning of internal organs such as liver, gallbladder, pancreas, and stomach. In addition, there are obvious morphological asymmetries in the brains of some vertebrates and functional left-right asymmetries in the activities of the brain, as assessed by psychological testing, MRI, and the analysis of lesions. There are several fundamental questions: What are the origins of the left-right axis, and are they highly conserved across metazoans? Once the left-right axis is established by the initial breaking of bilateral symmetry, what is the genetic pathway that perpetrates left-right development? What are the cellular and tissue mechanics that lead to morphogenesis during, for example, the looping of the cardiac tube, the coiling of the gut, or asymmetric brain development? Finally, do the asymmetric developmental pathways of each organ system take register from the same initial event that establishes the left-right axis, or are there separate mechanisms that orient heart, gut, and brain left-right asymmetry with respect to the DV and AP axes? These questions are beginning to be experimentally addressed, and papers in this issue of Developmental Genetics make contributions to several aspects in the burgeoning field of left-right development. Recent reviews have summarized the emerging genes and pathways in vertebrate left-right development [Wood, 1997; Harvey, 1998; Ramsdell and Yost, 1998]. Here, I give an overview of the contributions in this issue to the fundamental questions in left-right development. Dev. Genet. 23:159–163, 1998. © 1998 Wiley-Liss, Inc.     

Social learning of a communicative signal in captive chimpanzees

The acquisition of linguistic competency from more experienced social partners is a fundamental aspect of human language. However, there is little evidence that non-human primates learn to use their vocalizations from social partners. Captive chimpanzees (Pan troglodytes) produce idiosyncratic vocal signals that are used intentionally to capture the attention of a human experimenter. Interestingly, not all apes produce these sounds, and it is unclear what factors explain this difference. We tested the hypothesis that these attention-getting (AG) sounds are socially learned via transmission between mothers and their offspring. We assessed 158 chimpanzees to determine if they produced AG sounds. A significant association was found between mother and offspring sound production. This association was attributable to individuals who were raised by their biological mother-as opposed to those raised by humans in a nursery environment. These data support the hypothesis that social learning plays a role in the acquisition and use of communicative vocal signals in chimpanzees.